1174 Original Article MORPHOLOGICAL CHARACTERISTICS OF THE TONGUE OF THE ROCK CAVY- Kerodon rupestris WIED, 1820 (Rodentia, Caviidae)

CARACTERÍSTICAS MORFOLÓGICAS DA LÍNGUA EM MOCÓS- Kerodon rupestris WIED, 1820 (Rodentia,Caviidae)

Amilton Cesar dos SANTOS 1; Marian Mazeto de ARO 2; Bruno Machado BERTASSOLI 3; Diego Carvalho VIANA 1; Bruno Gomes VASCONCELOS 4; Rose Eli Grassi RICI 5; Moacir Franco de OLIVEIRA 6; Maria Angélica MIGLINO 5; Antônio Chaves de ASSIS-NETO 5 1. Doutorandos, Faculdade de Medicina Veterinária e Zootecnia- FMVZ. Universidade de São Paulo - USP, São Paulo, SP, Brasil. [email protected], [email protected]; 2. Graduanda, Faculdade de Medicina Veterinária e Zootecnia- FMVZ. Universidade de São Paulo - USP, São Paulo, SP, Brasil; 3. Doutorando, Universidade Federal de Minas Gerais- UFMG, Belo Horizonte, MG, Brasil; 4. Professor Doutor, Universidade Federal de Mato Grosso - UFMT, Sinop, MT, Brasil; 5. Professores Doutores, Faculdade de Medicina Veterinária e Zootecnia – FMVZ - USP, São Paulo, SP, Brasil; 6. Professor, Doutor, Universidade Federal Rural do Semiárido - UFERSA, Mossoró, RN, Brasil;

ABSTRACT: The Kerodon rupestris are wild rodents bred in captivity in order to their conservation and development of researches. The aim of this study was describe the morphology of the tongue from eight animals by light microscopy and scanning electron microscopy, beyond macroscopic studies. The tongues of K. rupestris had 3.15 ± 0.28 cm of length; 1.0 ± 0.20 cm width at the root; 0.38 ± 0.10 cm width at the body; and, 1.10 ± 0.09 cm width at the apex. Thickness measurements were 0.50 ± 0.09 cm at the apex; 0.30 ± 0.10 cm at the body; and, 0.70 ± 0.10 cm at the root. The free apex had 0.50 ± 0.10 cm in length. The dorsal surface of the tongue contained the fungiform and filiform papillae at the apex and body; conical papillae and a pairs of vallate papillae at the root, and foliated papillae dorsolaterally positioned in the root region. The proper lamina of the dorsal surface of the tongue was composed by keratinized stratified squamous epithelium, in which lingual papillae were found; and, a rich network of skeletal striated muscle and non-modeled dense connective tissue, in which vessels, nerves, mucous and serous acini and their respective ducts were found. In summary, dorsal surface of the tongue of K. rupestris had filiform and conical papillae with mechanical function, and, fungiform, vallate and foliated papillae with taste buds responsible by gustatory function. Moreover, the tongue of these animals showed some peculiarities as the eminence on the apex in sagittal plane, which needs further studies.

KEYWORDS: Digestory apparatus. Lingual papillae. Oral cavity. Wild rodents.

INTRODUCTION development of researches (OLIVEIRA et al., 2011; SANTOS et al., 2014). The rock cavies Kerodon rupestris are wild In this sense, few studies focusing on the rodents, which have been restricted to the semiarid digestory apparatus of the K. rupestris have been region of Caatinga in the Brazilian Northeastern. published and they described teeth (THOMAZ et They belong to the Caviidae family, Caviinae al., 2006) and stomach (BORSARI et al., 2010) subfamily (ADRIAN; SACHSER, 2011; morphology. Another important organ of digestory RODRIGUES et al., 2013) and Kerodon genus apparatus is the tongue, in which, different types of (THOMAZ et al., 2006). Their habit consist of functional lingual papillae (WITT; REUTTER, stalking in the afternoon or at night to seek leaves, 1997; BRANCO et al., 2011, 2012; buds, twigs, fruits, bark, roots and tubers from the MANÇANARES et al., 2012) lie on the dorsum, shrubs of the Caatinga (OLIVEIRA et al., 2011). and are variously distributed in different vertebrate The Caviidae are prey of most South species (IWASAKI, 2002; JACKOWIAK; American predators and thus they have important GODYNICKI, 2005; NONAKA; ZHENG; ecological role in the food chain. Moreover, the K. KOBAYASHI, 2008). The aim of this study was rupestris are subject to intense hunting due to their describe the morphological characteristics of the size and tasty meat, which is greatly appreciated by tongue of K. rupestris , providing more data for the rural population in the Brazilian Northeastern future researches. (ZOGNO; MIGLINO; OLIVEIRA, 2004). For this reason, K. rupestris and other Brazilian Caviidae are bred in captivity in order to provide alternative source of proteins, preserve the species and to

Received: 09/04/14 Biosci. J., Uberlândia, v. 31, n. 4, p. 1174-1182, July/Aug. 2015 Accepted: 15/10/14 1175 Morphological characteristics... SANTOS, A. C.

MATERIAL AND METHODS tissues were washed with buffer solution and dehydrated in increasing ethanol series (from 50 to Animals 100%), followed by critical point drying (Balzers Tongues of four males and four females PCD 020). Then, the fragments were properly fixed (adults and healthy) from the Breeding Center in metallic (stubs) and coated in gold (Emitech (CEMAS) of the Federal Rural University of the K550). The analysis was performed with electron Semiarid Region (UFERSA), Mossoró RN Brazil microscope Leo 435 VP (Semtech, USA). (IBAMA 2028236/2008) were used in present study. The study was approved by the Bioethics Light Microscopy Analysis (LM) Committee of the School of Veterinary Medicine From the tongues fixed in 10% and Animal Science, University of São Paulo, São formaldehyde, samples of apex, body, root and Paulo SP Brazil (n o 2485/2011). The animals came lateral regions of the root were extracted. Then, the from other previous studies and they had already fragments were dehydrated in increasing series of been euthanized and fixed in formaldehyde 10% ethanol (from 70 to 100%) and diaphanized in (four animals) and glutaraldehyde 2.5% 0.1M (four xylene for inclusion in paraffin blocks. Cuts with animals). 5µm in Leica RM 2155 microtome were obtained and stained with hematoxylin and eosin (HE) in Macroscopic Analysis order to analyze the microscopic morphology of the The tongues were dissected, removed and tongue. BX61VS Olympus photomicroscope was then, total length, width and thickness at the apex, used for microscopic photodocumentation. body and root were obtained with digital calipers (Mitotuyo, Tokyo, Japan). So, a schematic drawing RESULTS of the morphology of the tongue for a better view of your shape was performed. The measurements of Macroscopic analysis mean and standard deviation were performed. The tongues of K. rupestris had 3.15 ± 0.28 Photodocumentation was performed by camera cm of length; 1.0 ± 0.20 cm width at the root; 0.38 ± Olympus SP 810UZ 14 mp. 0.10 cm width at the body; and, 1.10 ± 0.09 cm width at the apex. Thickness measurements were Scanning Electron Microscopy Analysis (SEM) 0.50 ± 0.09 cm at the apex; 0.30 ± 0.10 cm at the The tongues fixed in glutaraldehyde 2.5% body; and, 0.70 ± 0.10 cm at the root. The free apex 0.1M (pH 7.4) were sectioned into three parts: root, had 0.5 ± 0.10 cm of length (Figure 1A and B). body and apex. Then, the fragments were washed Morphologically, an intermolar eminence at the root with 0.1 M phosphate buffer solution and post-fixed and a lower eminence in the sagittal plane at the in osmium tetroxide (Spurr's Kit-Electron apex were noted (Figure 1A and B; 2A). Microscopy Sciences Co., USA). The fragments of

Figure 1. Illustration of the anatomical shape and measurements of the tongue of K. rupestris . A: shape and measurements of length and width at the apex (a), body (b), and root (r). B: shape and measurements of length and thickness at the apex (a), body (b), and root (r).

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Scanning Electron Microscopy Analysis (SEM) was scattered among the filiform papillae at the By SEM, we observed that the dorsum of body and apex (Figure 2D). A pair of vallate the tongue had several filiform papillae scattered papillae with rectilinear grooves at the root was throughout the body and apex (Figure 2D); conical present (Figure 2B). Foliate papillae at the root was papillae was scattered in the region of the intermolar dorsum-laterally positioned (Figure 2C). eminence at root (Figure 2B); fungiform papillae

Figure 2. Photography and electron micrograph of the tongue of K. rupestris . A: Photograph showing root (r), body (b), and apex (a) and median eminence (*) at the apex. B: electron micrograph showing vallate (circle) and conical papillae (arrow) at the root. Bar: 1 mm. C: electron micrograph from lateral view of root showing foliated papillae (arrow) and vallate papillae (arrowhead). Bar: 1 mm. D: electron micrograph showing foliated papillae at the body. Bar: 100 µm. E: electron micrograph at the body showing fungiform papillae (f) surrounded by filiform papillae. Bar: 100 µm.

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Light Microscopy Analysis (LM) squamous epithelium in the ventral surface of The proper lamina of the dorsal surface of tongue was found (Figure 3C and D). the tongue was composed by the surface covered Unilocular adipose tissue was found with keratinized stratified squamous epithelium, in between muscular bundles (Figure 3D). The ventral which several papillae were found and non-modeled surface of the tongue had keratinized stratified dense connective tissue, in which vessels, nerves, squamous epithelium and absence of lingual mucous and serous acini and their respective ducts papillae (Figure 3C). were found (Figure 3A, B, E and F; Figure 4A and The fungiform (Figure 3B), foliated (Figure B). Moreover, a rich network of skeletal striated 4B and C) and vallate papillae (Fig. 3E) had taste muscle, with longitudinal, transversal and circular buds (Figure 3E). In the region of the vallate and fibers over its entire length and keratinized stratified foliated papillae, serous and mucous acini were found (Figure 3E and F; 4B).

Figure 3. Photomicrograph of the tongue of K. rupestris stained with HE. A: filiform papillae (arrow) lined by keratinized (k) stratified epithelium (e), connective tissue (ct), and muscular layers (m). Bar: 500 µm. B: fungiform papillae lined by keratinized (arrow) stratified epithelium (e), and taste bud (arrowhead), a blood vessel (dotted circle) in the non-modeled dense connective tissue (ct). Bar: 200 µm. C: stratified epithelium (e), non-modeled dense connective tissue (ct) and muscular layers (m) at the ventral region of the tongue. Bar: 200 µm. D: circular (cm), longitudinal (lm), and transversal (tm) muscular layers and unilocular adipose tissue (*). Bar: 500 µm. E: vallate papillae (dotted arrow) with taste buds (arrow) and serous acini (circle) with ducts (arrowhead) in the connective tissue. Bar: 200 µm. F: serous (s) and mucous (m) acini. Bar: 200 µm.

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Figure 4. Photomicrograph of the tongue of K. rupestris stained with HE. A: conical papillae (arrows); keratinized stratified epithelium (e); connective tissue (ct) and muscular layer (m). Bar: 500 µm. B: foliated papillae (f); taste bud with its taste pore (dotted arrow) and blood vessels (arrow). Bar: 200 µm. C: transversal cut of foliated papillae (f) with their taste buds with taste pore (arrow) and papillary groove (g). Bar: 100 µm.

DISCUSSION The median groove found on the apex of tongue of the rodents Clethrionomys glareolus The tongue of K. rupestris is an organ with (JACKOWIAK; GODYNICKI, 2005), Sciurus a rich skeletal striated muscular layer, characterized vulgaris (ÜNSALDI, 2010 ), Spalax ehrenbergi by an intermolar eminence in the root region, as (KILINC et al., 2010), Arvicanthis niloticus (NASR; described in other rodents, as Cavia porcellus GAMAL; ELSHEIKH, 2012), Hystrix cristata (IWASAKI; MIYATA, 1985; KOBAYASHI, (KARAN; YILMAZ; AYDIN, 2011) and rats 1990), Clethrionomys glareolus (JACKOWIAK; (IWASAKI; YOSHIZAWA; KAWAHARA, 1997) GODYNICKI, 2005), Castor canadensis (SHINDO; was not found in K. rupestris , on the other hand, a YOSHIMURA; KOBAYASHI, 2006), Hystrix sagittal eminence was present in this region. cristata (KARAN et al., 2011), Sciurus vulgaris References to these structures were not found in (ÜNSALDI, 2010), Arvicanthis niloticus (NASR; other rodents, but these eminences could be related GAMAL; ELSHEIKH, 2012) and in lagomorph to the anatomy and physiology of mastication and Oryctolagus cuniculus (NONAKA; ZHENG; swallowing (CHENG et al., 2002). In this sense, we KOBAYASHI, 2008). Shindo, Yoshimura and believe that these eminences may be important to Kobayashi (2006) and Nonaka, Zheng and capture food by assisting incisor teeth. In addition, Kobayashi (2008) also reported that the intermolar these eminences may reflect adjustments in the bony eminence may be found in artiodactyls, rodents, structures of the palate. So, further studies of the rabbits and marsupials, and all these species have oral cavity in K. rupestris are needed, in order to herbivorous food habit. Silva, Watanabe and Kronka elucidate the importance of these eminences to the (2002) named the intermolar eminence as torus in capture, mastication and swallowing process of Oryctolagus cuniculus . food.

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The lingual papillae of K. rupestris were Five types of lingual papillae were found in irregularly distributed on the dorsal surface of the K. rupestris : filiform, conical, fungiform, foliated tongue, as described in Cavia porcellus and vallate. However, some studies in other rodent (KOBAYASHI, 1990), in wild carnivores as Nasua species do not cite foliated or conical papillae nasua (SOUZA et al., 2012.), in marsupials as (UTIYAMA et al., 1995; SHINDO; YOSHIMURA; Didelphis marsupialis (MANÇANARES et al., KOBAYASHI, 2006; ÜNSALDI, 2010; EMURA et 2012.); in domestic mammals as Felis catus and al., 2011). In Cavia porcellus , coronal papillae are Oryctolagus cuniculus (CHAMORRO et al., 1987); described on the intermolar eminence (IWASAKI; and, primates as Saimiri sciureus (BRANCO et al., MIYATA, 1985). To aid understanding the different 2011.) and Callithrix penicillata (BRANCO et al., distributions of the lingual papillae in different 2012), besides other non-mammalian vertebrates species, Table 1 shows their distribution in several such as amphibians, reptiles and birds (IWASAKI, rodents and non-rodents species. 2002).

Table 1. Lingual papillae available in rodents and other mammals. Specie/author Types of papillae Rodentia Filiform Fungiform Foliated vallate conical (n) Current research + + + + (2) + Cavia porcellus (KOBAYASHI, 1990) + + + ? + Clethrionomys glareolus (JACKOWIAK and + + + + (1) + GODYNICKI, 2005) Dolichotis patagonum (EMURA et al., 2011) + + + + (2) - Castor Canadensis (SHINDO et al., 2006) + + + + (3) - Sciurus vulgaris (ÜNSALDI, 2010) + + + + (3) - Calomys callosus (UTIYAMA et al., 1995) + + + + (1) - Spalax ehrenbergi (KILINC et al., 2010) + + - + (2) - Arvicanthis niloticus (NASR et al., 2012) + + - + (2) - No Rodentia Didelphis marsupialis (MANÇANARES et al., + + - + (3) - 2012) Oryctolagus cuniculus (SILVA et al., 2002; + + + + (2) - NONAKA et al., 2008) Nasua nasua (SOUZA et al., 2012) + + - + (9) + Felis catus (CHAMORRO et al., 1987) + + + + (6) + Callithrix penicillata (BRANCO et al., 2012) + + - + (3) - Saimiri sciureus (BRANCO et al., 2011) + + + + (3) - + = present/ - = absent/ ? = not described

In present study, the vallate papillae had and serous acini found in the same tongue of K. rectilinear grooves, but in other rodents as rupestris were not described in these above Clethrionomys glareolus (JACKOWIAK; described species. GODYNICKI, 2005), these papillae have V-shaped By histology, taste buds present in format. In Spalax ehrenbergi (KILINC et al., 2010) fungiform papillae of the tongue of K. rupestris and Calomys callosus (UTIYAMA et al., 1995), were described in other rodents, such as Castor they have an oval shape, surrounded by a deep canadensis (SHINDO; YOSHIMURA; groove. The vallate papillae of K. rupestris still had KOBAYASHI, 2006) and Sciurus vulgaris many taste buds as described in lagomorphs (ÜNSALDI, 2010). Oryctolagus cuniculus (NONAKA; ZHENG; The many foliated papillae with taste buds KOBAYASHI, 2008), in wild carnivores Nasua found in our study are also reported by Kobayashi Nasua (SOUZA et al., 2012), in marsupials (1990) in Cavia porcellus . Shindo, Yoshimura and Didelphis marsupialis (MANÇANARES et al., Kobayashi (2006) and Emura et al. (2011) reported 2012) and human (WITT; REUTTER, 1997). that the development of foliated papillae in rodents Nonaka, Zheng and Kobayashi (2008) reported that is related to wide variety of food. the vallate papillae are present in varying numbers, Keratinization found on the dorsal surface from one in mice and rats up to 10-20 in cattle, of the tongue of K. rupestris is also described in sheep, goats and deer. On the other hand, mucous other rodents that inhabit environments with low

Biosci. J., Uberlândia, v. 31, n. 4, p. 1174-1182, July/Aug. 2015 1180 Morphological characteristics... SANTOS, A. C. humidity, as Clethrionomys glareolus responsible for gustatory function. Moreover, the (JACKOWIAK; GODYNICKI, 2005), Hystrix tongue of these animals shows some peculiarities as cristata (KARAN; YILMAZ; AYDIN, 2011) and the intermolar eminence and another eminence in Dolichotis patagonum (EMURA et al., 2011). sagittal plane at the apex, which needs further Future studies may contrast the keratinization of the studies. tongue from animals that inhabit dry and wet climate, in order to extract better conclusions on this ACKNOWLEDGEMENTS point. We conclude that the dorsal surface of the The authors would like to thank the tongues of K. rupestris had filiform and conical Fundação de Amparo à Pesquisa do Estado de São papillae with mechanical function, and, fungiform, Paulo (FAPESP) for its financial support in current vallate and foliated papillae with taste buds research.

RESUMO: Os Kerodon rupestris são roedores silvestres criados em cativeiro para sua conservação e desenvolvimento de pesquisas. O objetivo deste estudo foi descrever a língua destes animais por meio de microscopia de luz, microscopia eletrônica de varredura e estudos macroscópicos. As línguas de K. rupestris tinham 3,15 ± 0,28 cm de comprimento; 1,00 ± 0,20 cm de largura na raiz, 0,38 ± 0,10 cm de largura no corpo e 1,10 ± 0,09 de largura no ápice. As medidas de espessura foram 0,50 ± 0,09 cm no ápice, 0,30 ± 0,10 cm no corpo e 0,70 ± 0,10 cm na raíz. O ápice livre possuía 0,50 ± 0,10 cm de comprimento. A superfície dorsal da língua continha papilas fungiformes e filiformes no ápice e corpo; papilas cônicas e um par de papilas valadas na raiz; e, papilas foliadas posicionadas dorsolateralmente na região da raiz. A lâmina própria da superfície dorsal da língua estava composta por epitélio estratificado pavimentoso queratinizado, no qual as papilas linguais foram encontradas; e, uma rica rede de músculo estriado esquelético e tecido conjuntivo denso não modelado, no qual veias, nervos e ácinos serosos e mucosos e seus respectivos ductos foram encontrados. Em conclusão, a superfície da língua de K. rupestris apresentou papilas filiformes e cônicas com função mecânica e papilas fungiformes, valadas e foliadas com botões gustativos responsáveis pela função gustativa. Além disso, a língua desses animais apresentou ainda particularidades, como uma eminência no plano sagital do ápice que necessita de futuros estudos.

PALAVRAS CHAVE: Aparelho digestório. Cavidade Oral. Papilas linguais. Roedores silvestres.

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